Skip to main content
SpringerLink
Log in

Interneuron Heterogeneity in Neocortex

  • Chapter
Excitatory-Inhibitory Balance

Abstract

Complex behavior and cognitive functions, such as perception, attention and memory, are believed to be intimately associated with the ~1–2 mm thin neocortical sheet, that forms the outer envelope of mammalian brains1, 2. Neocortical function is believed to ultimately arise from the communication among the intricately interconnected constituent excitatory and inhibitory neurons3–9. In the late 1950’s and early 1960’s, experiments revealed small repeating functional units of several thousand cells, that are vertically arranged into cylinders/slabs (traversing all cortical layers) of about half a millimeter in diameter10,11. Functional modules, as exemplified by these cortical columns, have been found in many neocortical areas, establishing the notion that the neocortical sheet may be viewed as a mosaic of small repeating modules1,7,8,12–18. Understanding the structure and function of these modules, therefore, provides the foundation for understanding neocortical function.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Mountcastle V. B. (1998) Perceptual Neuroscience: the Cerebral Cortex (Harvard University Press, Cambridge)

    Google Scholar 

  2. Kandel E., Schwartz J. H. and Jessel T. M. (2001) Principles in Neural Science, 4th ed., Aplleton and Lange, Norwalk

    Google Scholar 

  3. Cajal S. R. (1909) Histology due systeme nerveux de homme et des vertebrates Maloine, Paris

    Google Scholar 

  4. Lorente de No R. (1938) Cerebral cortex: architecture, intracortical connections, motor projections. In: Physiology of the nervous system, pp. 291–329, Fulton J. F., ed. (1st. Oxford University Press, NY)

    Google Scholar 

  5. Mountcastle V. B. (1978) An organizing principle for cerebral function: the unit module and the distributed system. In The mindful brain : cortical organization and the group-selective theory of higher brain function, pp. 7 - 50, Edelman G. M. and Mountcastle V. B. (eds.), MIT Press,

    Google Scholar 

  6. Szentagothai J. (1978) The Ferrier Lecture, 1977. The neuron network of the cerebral cortex: a functional interpretation. Proc R Soc Lond B Biol Sci 201: 219–248.

    PubMed  CAS  Google Scholar 

  7. Eccles J. C. (1984) The Cerebral neocortex: a theory of its operation. In: Cerebral cortex: functional properties of cortical cells, Vol. 2, pp. 1–38, Jones E. G. and Peters A., eds. (Plenum Press, New York)

    Google Scholar 

  8. Shepherd G. M. (1988) A basic circuit of cortical organization. In: Perspectives in memory research, Gazzaniga, ed. (MIT Press, Cambridge), pp. 93–134

    Google Scholar 

  9. Douglas R. and Martin K. A. C. (1998) Neocortex. In: The synaptic organization of the brain, pp. 459–511, Shepherd G. M., eds. (Oxford University Press, New York)

    Google Scholar 

  10. Mountcastle V. B. (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J. Neurophysiology 20: 408–434.

    CAS  Google Scholar 

  11. Hubel D. H. and T.N. W. (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160: 106–154.

    PubMed  CAS  Google Scholar 

  12. Jones E. G., Burton H. and Porter R. (1975) Commissural and cortico-cortical “columns” in the somatic sensory cortex of primates. Science 190: 572–574.

    PubMed  CAS  Google Scholar 

  13. Goldman P. S. and Nauta W. J. (1977) Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey. Brain Res 122: 393–413.

    PubMed  CAS  Google Scholar 

  14. Goldman-Rakic P. S. and Schwartz M. L. (1982) Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. Science 216: 755–757.

    PubMed  CAS  Google Scholar 

  15. Szentagothai J. (1983) The modular architectonic principle of neural centers. Rev Physiol Biochem Pharmacol 98: 11–61.

    PubMed  CAS  Google Scholar 

  16. Purves D., Riddle D. R. and LaMantia A. S. (1992) Iterated patterns of brain circuitry (or how the cortex gets its spots). Trends Neurosci 15: 362–368.

    PubMed  CAS  Google Scholar 

  17. White E. L. (1989) Cortical Circuits. Synaptic Organization of the Cerebral Cortex Birkhauser, Boston

    Google Scholar 

  18. Tanaka K. (1997) Columnar Organization in the Inferotemporal Cortex. In: Cerebral Cortex : Extrastriate Cortex in Primates, Vol. 12, pp. 469–498, Rockland K. S. ,Kaas J. H. and Peters A. (eds.), Plenum Press, New York

    Google Scholar 

  19. DeFelipe J. and Farinas I. (1992) The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol 39: 563–607.

    PubMed  CAS  Google Scholar 

  20. Jones E. G. (1984) Laminar distribution of cortical efferent cells. In: Cellular Components of the Cerebral Cortex, Vol. 1, pp. 521–554, Peters A. and Jones E. G. (eds.), Plenum Press, New York

    Google Scholar 

  21. Peters A. and Jones E. G. (1984) Cellular Componenets of the Cerebral Cortex Plenum Press, New York

    Google Scholar 

  22. DeFelipe J. (1993) Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb Cortex 3: 273–289.

    PubMed  CAS  Google Scholar 

  23. Kawaguchi Y. and Kubota Y. (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7: 476–486.

    PubMed  CAS  Google Scholar 

  24. Cauli B. et al. (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17: 3894–3906.

    PubMed  CAS  Google Scholar 

  25. Toledo-Rodriguez M, Gupta A., Wang Y., Wu C. Z. and Markram H. (2003) Neocortex: basic neuron types. In: The Handbook of Brain Theory and Neural Networks. Arbib M. A. (ed.), 2nd ed., MIT Press, Cambridge

    Google Scholar 

  26. Peters A. (1987) Synaptic Specificity in the cerebral cortex. In: Synaptic Function, pp. 373–397, Edelman G. M. ,Gall W. E. and Cowan J. (eds.), Wiley-Press, New York

    Google Scholar 

  27. Somogyi P., Tamas G., Lujan R. and Buhl E. H. (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26: 113–135.

    PubMed  CAS  Google Scholar 

  28. Gupta A., Wang Y. and Markram H. (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273–278.

    PubMed  CAS  Google Scholar 

  29. Ren J. Q., Aika Y., Heizmann C. W. and Kosaka T. (1992) Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons. Exp Brain Res 92: 1–14.

    PubMed  CAS  Google Scholar 

  30. Beaulieu C. (1993) Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res 609: 284–292.

    PubMed  CAS  Google Scholar 

  31. Houser C. R., Vaughn J. E., Hendry S. H. C., Jones E. G. and Peters A. (1984) GABA neurons in the cerebral cortex. In: Cerebral cortex: functional properties of cortical cells, Vol. 2, pp. 63–90, Jones E. G. and Peters A. (eds.), Plenum Press, New York

    Google Scholar 

  32. DeFelipe J. (2002) Cortical interneurons: from Cajal to 2001. Prog Brain Res 136: 215–238

    PubMed  Google Scholar 

  33. Peters A., Palay S. L. and Webster H. D. (1991) The fine structure of the nervous system, 3rd ed., Oxford University Press, New York

    Google Scholar 

  34. Peters A. and Jones E. G. (1984) Classification of cortical neurons. In: Cellular Components of the Cerebral Cortex, Vol. 1, pp. 107–122, Peters A. and Jones E. G. (eds.), Plenum Press, New York

    Google Scholar 

  35. Somogyi P. (1989) Synaptic organisation of GABAergic neurons and GABAa receptors in the lateral geniculate nucleus and visual cortex. In: Neuronal Mechanisms of Visual Perception, Proc Retina Res Found Symp, 2, pp. 35–62, Lamm D. K. T. and Gilbert C. D. (eds.), Portfolio Publ., Woodlands, Texas

    Google Scholar 

  36. Marin-Padilla M. (1984) Neurons of layer I: a developmental analysis. In: Cellular Components of the Cerebral Cortex, Vol. 1Peters A. and Jones E. G. (eds.), Plenum Press, New York

    Google Scholar 

  37. DeFelipe J. (1997) Microcircuits in the brain. In: Biological and artificial computation. lecture notes in computer science, Vol. 1240, pp. 1–14, Mira J. ,Moreno-Diaz R. and Cabestany J. (eds.), Springer Verlag, Berlin

    Google Scholar 

  38. Wang Y., Gupta A., Toledo-Rodriguez M., Wu C. Z. and Markram H. (2002) Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12: 395–410.

    PubMed  Google Scholar 

  39. Tarczy-Homoch K., Martin K. A., Jack J. J. and Stratford K. J. (1998) Synaptic interactions between smooth and spiny neurones in layer 4 of cat visual cortex in vitro. J Physiol 508: 351–363.

    Google Scholar 

  40. Kisvarday Z. F. (1992) GABAergic networks of basket cells in the visual cortex. Prog Brain Res 90: 385–405.

    PubMed  CAS  Google Scholar 

  41. Callaway E. M. (1998) Local circuits in primary visual cortex of the macaque monkey. Annu Rev Neurosci 21: 47–74.

    PubMed  CAS  Google Scholar 

  42. Jones E. G. (1975) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J Comp Neurol 160: 205–267.

    PubMed  CAS  Google Scholar 

  43. Gilbert C. D. (1993) Circuitry, architecture, and functional dynamics of visual cortex. Cereb Cortex 3: 373–386.

    PubMed  CAS  Google Scholar 

  44. Keller A. (1993) Intrinsic synaptic organization of the motor cortex. Cereb Cortex 3: 430–441.

    PubMed  CAS  Google Scholar 

  45. Lund J. S. (1988) Anatomical organization of macaque monkey striate visual cortex. Annu Rev Neurosci 11: 253–288.

    PubMed  CAS  Google Scholar 

  46. O’Leary J. L. (1941) Structure of the area striate of the cat. J.Comp.Neurol. 75: 131–163

    Google Scholar 

  47. Valverde F. (1986) Intrinsic neocortical organization: some comparative aspects. Neuroscience 18:1–23.

    PubMed  CAS  Google Scholar 

  48. Feldman M. L. and Peters A. (1978) The forms of non-pyramidal neurons in the visual cortex of the rat. J Comp Neurol 179: 761–793.

    PubMed  CAS  Google Scholar 

  49. Martin K. A. C. (1984) Neuronal circuits in cat striate cortex. In: Cerebral cortex: functional properties of cortical cells, Vol. 2, pp. 241–284, Jones E. G. and Peters A. (eds.), Plenum Press, New York

    Google Scholar 

  50. Peters A. and Fairen A. (1978) Smooth and sparsely-spined stellate cells in the visual cortex of the rat: a study using a combined Golgi-electron microscopic technique. J Comp Neurol 181: 129–171.

    PubMed  CAS  Google Scholar 

  51. Jones E. G. and Hendry S. H. C. (1984) Basket cells. In: Cellular Components of the Cerebral Cortex, Vol. 1, pp. 309–336, Peters A. and Jones E. G. (eds.), Plenum Press, New York

    Google Scholar 

  52. Marin-Padilla M. (1969) Origin of the pericellular baskets of the pyramidal cells of the human motor cortex: a Golgi study. Brain Res 14: 633–646.

    PubMed  CAS  Google Scholar 

  53. Marin-Padilla M. (1970) Prenatal and early postnatal ontogenesis of the human motor cortex: a golgi study. II. The basket-pyramidal system. Brain Res 23: 185–191.

    PubMed  CAS  Google Scholar 

  54. Marin-Padilla M. and Stibitz G. R. (1974) Three-dimensional reconstruction of the basket cell of the human motor cortex. Brain Res 70: 511–514.

    PubMed  CAS  Google Scholar 

  55. Szentagothai J. (1973) Synaptology of the visual cortex. In: Central Processing of Visual Information, B. Visual Centers in the Brain, pp. 269–324, Jung R. (ed.), Springer-Verlag, Berlin

    Google Scholar 

  56. Kisvarday Z. F., Martin K. A., Whitteridge D. and Somogyi P. (1985) Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat. J Comp Neurol 241: 111–137.

    PubMed  CAS  Google Scholar 

  57. Somogyi P. (1977) A specific ’axo-axonal’ interneuron in the visual cortex of the rat. Brain Res 136: 345–350.

    PubMed  CAS  Google Scholar 

  58. Somogyi P., Freund T. F. and Cowey A. (1982) The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience 7: 2577–2607.

    PubMed  CAS  Google Scholar 

  59. Fairen A., DeFelipe J. and Regidor J. (1984) Nonpyramidal Neurons; general account. In: Cellular Components of the Cerebral Cortex, Vol. 1Peters A. and Jones E. G. (eds.), m, New York

    Google Scholar 

  60. Wu C. Z., Gupta A., Wang Y., Toledo-Rodriguez M., J.Y. L. and Markram H. (2001) Morphological, physiological, molecular and synaptic properties of Martinotti cells in rat somatosensory cortex. Neural Plast 8: 208–208.

    Google Scholar 

  61. Peters A. (1984) Bipolar cells. In: Cellular Components of the Cerebral Cortex, Vol. 1, pp. 381–408, Peters A. and Jones E. G. (eds.), Plenum Press, New York

    Google Scholar 

  62. Peters A. and Harriman K. M. (1988) Enigmatic bipolar cell of rat visual cortex. J Comp Neurol 267: 409–432.

    PubMed  CAS  Google Scholar 

  63. Peters A. (1990) The axon terminals of vasoactive intestinal polypeptide (VIP)-containing bipolar cells in rat visual cortex. J Neurocytol 19: 672–685.

    PubMed  CAS  Google Scholar 

  64. Somogyi P. and Cowey A. (1981) Combined Golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey. J Comp Neurol 195: 547– 566.

    PubMed  CAS  Google Scholar 

  65. Somogyi P. and Cowey A. (1984) Double bouquet cells. In: Cellular Components of the Cerebral Cortex, Vol. 1, pp. 337–360, Peters A. and Jones E. G. (eds.), Plenum Press, New York

    Google Scholar 

  66. DeFelipe J., Hendry S. H., Hashikawa T., Molinari M. and Jones E. G. (1990) A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37: 655–673.

    PubMed  CAS  Google Scholar 

  67. Jones E. G. (1984) Neurogliaform or spiderweb cells. In: Cellular Components of the Cerebral Cortex, Vol. 1, pp. 409–418, Peters A. and Jones E. G. (eds.), Plenum Press, New York

    Google Scholar 

  68. Hestrin S. and Armstrong W. E. (1996) Morphology and physiology of cortical neurons in layer I. J Neurosci 16: 5290–5300.

    PubMed  CAS  Google Scholar 

  69. Toemboel T. (1984) Layer VI cells. In: Cellular Components of the Cerebral Cortex, Vol. 1, pp. 479–520, Peters A. and Jones E. G. (eds.), Plenum Press, New York

    Google Scholar 

  70. McCormick D. A., Connors B. W., Lighthall J. W. and Prince D. A. (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782–806.

    PubMed  CAS  Google Scholar 

  71. Connors B. W. and Gutnick M. J. (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 99–104.

    PubMed  CAS  Google Scholar 

  72. Thomson A. M., West D. C., Hahn J. and Deuchars J. (1996) Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J Physiol 496: 81–102.

    PubMed  CAS  Google Scholar 

  73. Thomson A. M. and Deuchars J. (1997) Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb Cortex 7: 510–522.

    PubMed  CAS  Google Scholar 

  74. Kawaguchi Y. and Kubota Y. (1996) Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16: 2701–2715.

    PubMed  CAS  Google Scholar 

  75. Kawaguchi Y. and Kubota Y. (1998) Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85: 677–701.

    PubMed  CAS  Google Scholar 

  76. Porter J. T., Cauli B., Staiger J. F., Lambolez B., Rossier J. and Audinat E. (1998) Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex. Eur J Neurosci 10: 3617–3628.

    PubMed  CAS  Google Scholar 

  77. Amitai Y. and Connors B. W. (1995) Intrinsic physiology and morphology of single neurons in neocortex. In: Cerebral cortex: the barrel cortex of rodents, Vol. 11, pp. 299–331, Jones E. G. and Diamond I. T. (eds.), Plenum Press, New York

    Google Scholar 

  78. Gray C. M. and McCormick D. A. (1996) Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science 274: 109–113.

    PubMed  CAS  Google Scholar 

  79. Kawaguchi Y. and Kubota Y. (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70: 387–396.

    PubMed  CAS  Google Scholar 

  80. Kawaguchi Y. (1993) Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69: 416–431.

    PubMed  CAS  Google Scholar 

  81. Connors B. W., Gutnick M. J. and Prince D. A. (1982) Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48: 1302–1320.

    PubMed  CAS  Google Scholar 

  82. Cauli B. et al. (2000) Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci U S A 97: 6144–6149.

    PubMed  CAS  Google Scholar 

  83. DeFelipe J., Hendry S. H., Jones E. G. and Schmechel D. (1985) Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex. J Comp Neurol 231: 364–384.

    PubMed  CAS  Google Scholar 

  84. del Rio M. R. and DeFelipe J. (1995) A light and electron microscopic study of calbindin D-28k immunoreactive double bouquet cells in the human temporal cortex. Brain Res 690: 133–140.

    PubMed  Google Scholar 

  85. Larkum M. E., Zhu J. J. and Sakmann B. (2001) Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J Physiol 533: 447–466.

    PubMed  CAS  Google Scholar 

  86. Schiller J., Major G., Koester H. J. and Schiller Y. (2000) NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404: 285–289

    PubMed  CAS  Google Scholar 

  87. Segev I. and London M. (2000) Untangling dendrites with quantitative models. Science 290: 744–750.

    PubMed  CAS  Google Scholar 

  88. Hausser M., Spruston N. and Stuart G. J. (2000) Diversity and dynamics of dendritic signaling. Science 290: 739–744.

    PubMed  CAS  Google Scholar 

  89. Reyes A., Lujan R., Rozov A., Burnashev N., Somogyi P. and Sakmann B. (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279–285.

    PubMed  CAS  Google Scholar 

  90. Ahmed B., Anderson J. C., Martin K. A. and Nelson J. C. (1997) Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J Comp Neurol 380: 230–242.

    PubMed  CAS  Google Scholar 

  91. Buhl E. H., Tamas G., Szilagyi T., Stricker C., Paulsen O. and Somogyi P. (1997) Effect, number and location of synapses made by single pyramidal cells onto aspiny interneurones of cat visual cortex. J Physiol 500: 689–713.

    PubMed  CAS  Google Scholar 

  92. Thomson A. M., West D. C. and Deuchars J. (1995) Properties of single axon excitatory postsynaptic potentials elicited in spiny interneurons by action potentials in pyramidal neurons in slices of rat neocortex. Neuroscience 69: 727–738.

    PubMed  CAS  Google Scholar 

  93. Deuchars J. and Thomson A. M. (1995) Innervation of burst firing spiny interneurons by pyramidal cells in deep layers of rat somatomotor cortex: paired intracellular recordings with biocytin filling. Neuroscience 69: 739–755.

    PubMed  CAS  Google Scholar 

  94. Krimer L. S. and Goldman-Rakic P. S. (2001) Prefrontal microcircuits: membrane properties and excitatory input of local, medium, and wide arbor interneurons. J Neurosci 21: 3788–3796.

    PubMed  CAS  Google Scholar 

  95. Rozov A., Jerecic J., Sakmann B. and Burnashev N. (2001) AMPA receptor channels with long-lasting desensitization in bipolar interneurons contribute to synaptic depression in a novel feedback circuit in layer 2/3 of rat neocortex. J Neurosci 21: 8062–8071.

    PubMed  CAS  Google Scholar 

  96. Buhl E. H., Cobb S. R., Halasy K. and Somogyi P. (1995) Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7: 1989–2004.

    PubMed  CAS  Google Scholar 

  97. Miles R., Toth K., Gulyas A. I., Hajos N. and Freund T. F. (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16: 815–823.

    PubMed  CAS  Google Scholar 

  98. Cobb S. R., Buhl E. H., Halasy K., Paulsen O. and Somogyi P. (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75–78.

    PubMed  CAS  Google Scholar 

  99. Pouille F. and Scanziani M. (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feedforward inhibition. Science 293: 1159–1163.

    PubMed  CAS  Google Scholar 

  100. Larkum M. E., Zhu J. J. and Sakmann B. (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398: 338–341.

    PubMed  CAS  Google Scholar 

  101. Segev I. and Rall W. (1998) Excitable dendrites and spines: earlier theoretical insights elucidate recent direct observations. Trends Neurosci 21: 453–460.

    PubMed  CAS  Google Scholar 

  102. Segev I. and London M. (1999) A theoretical view of passive and active dendrites. In: Dendrites Stuart G. ,Spruston N. and Hausser M. (eds.), Oxford University Press,

    Google Scholar 

  103. Williams S. R. and Stuart G. J. (2002) Dependence of EPSP Efficacy on Synapse Location in Neocortical Pyramidal Neurons. Science 295: 1907–1910.

    PubMed  CAS  Google Scholar 

  104. Markram H., Lubke J., Frotscher M. and Sakmann B. (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275: 213–215.

    PubMed  CAS  Google Scholar 

  105. Magee J. C. and Johnston D. (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275: 209–213.

    PubMed  CAS  Google Scholar 

  106. Traub R. D. (1995) Model of synchronized population bursts in electrically coupled interneurons containing active dendritic conductances. J Comput Neurosci 2: 283–289.

    PubMed  CAS  Google Scholar 

  107. Tamas G., Buhl E. H. and Somogyi P. (1997) Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J Physiol 500: 715–738.

    PubMed  CAS  Google Scholar 

  108. Tamas G., Somogyi P. and Buhl E. H. (1998) Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J Neurosci 18: 4255–4270.

    PubMed  CAS  Google Scholar 

  109. Koch C. (1999) Biophysics of computation Oxford University Press, New York

    Google Scholar 

  110. Kisvarday Z. F., Beaulieu C. and Eysel U. T. (1993) Network of GABAergic large basket cells in cat visual cortex (area 18): implication for lateral disinhibition. J Comp Neurol 327: 398–415.

    PubMed  CAS  Google Scholar 

  111. Tamas G., Buhl E. H., Lorincz A. and Somogyi P. (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3: 366–371.

    PubMed  CAS  Google Scholar 

  112. Fukuda T. and Kosaka T. (2000) The dual network of GABAergic interneurons linked by both chemical and electrical synapses: a possible infrastructure of the cerebral cortex. Neurosci Res 38: 123–130.

    PubMed  CAS  Google Scholar 

  113. Gibson J. R., Beierlein M. and Connors B. W. (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75–79.

    PubMed  CAS  Google Scholar 

  114. Beierlein M., Gibson J. R. and Connors B. W. (2000) A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3: 904–910.

    PubMed  CAS  Google Scholar 

  115. Galarreta M. and Hestrin S. (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402: 72–75.

    PubMed  CAS  Google Scholar 

  116. Galarreta M. and Hestrin S. (2001) Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2: 425–433.

    PubMed  CAS  Google Scholar 

  117. McBain C. J. and Fisahn A. (2001) Interneurons unbound. Nat Rev Neurosci 2:11–23.

    PubMed  CAS  Google Scholar 

  118. Thomson A. M. (2000) Neurotransmission: Chemical and electrical interneuron coupling. Curr Biol 10: Rl10–112.

    Google Scholar 

  119. Hestrin S. (1993) Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons. Neuron 11: 1083–1091.

    PubMed  CAS  Google Scholar 

  120. Thomson A. M, Deuchars J. and West D. C. (1996) Neocortical local synaptic circuitry revealed with dual intracellular recordings and biocytin-filling. J Physiol Paris 90: 211–215.

    PubMed  CAS  Google Scholar 

  121. Thomson A. M., Deuchars J. and West D. C. (1993) Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation. Neuroscience 54: 347–360.

    PubMed  CAS  Google Scholar 

  122. Thomson A. M. (1997) Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J Physiol 502: 131–147.

    PubMed  CAS  Google Scholar 

  123. Markram H., Wang Y. and Tsodyks M. (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 95: 5323–5328.

    PubMed  CAS  Google Scholar 

  124. Wang Y., Gupta A. and Markram H. (1999) Anatomical and functional differentiation of glutamatergic synaptic innervation in the neocortex. J Physiol Paris 93: 305–317.

    PubMed  CAS  Google Scholar 

  125. Gupta A., Wang Y. and Markram H. (2001) Principles of neocortical interneuron recruitment. Neural Plast 8: 176–176

    Google Scholar 

  126. Angulo M. C., Rossier J. and Audinat E. (1999) Postsynaptic glutamate receptors and integrative properties of fast-spiking interneurons in the rat neocortex. J Neurophysiol 82: 1295–1302.

    PubMed  CAS  Google Scholar 

  127. Galarreta M. and Hestrin S. (1998) Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1: 587–594.

    PubMed  CAS  Google Scholar 

  128. Rozov A., Burnashev N., Sakmann B. and Neher E. (2001) Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531: 807–826.

    PubMed  CAS  Google Scholar 

  129. Thomson A. M. and Bannister A. P. (1999) Release-independent depression at pyramidal inputs onto specific cell targets: dual recordings in slices of rat cortex. J Physiol 519: 57–70.

    PubMed  CAS  Google Scholar 

  130. Deuchars J. and Thomson A. M. (1995) Single axon fast inhibitory postsynaptic potentials elicited by a sparsely spiny interneuron in rat neocortex. Neuroscience 65: 935–942.

    PubMed  CAS  Google Scholar 

  131. Nicoll R. A., Malenka R. C. and Kauer J. A. (1990) Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol Rev 70: 513–565.

    PubMed  CAS  Google Scholar 

  132. Thomson A. M. and Destexhe A. (1999) Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices. Neuroscience 92: 1193–1215.

    PubMed  CAS  Google Scholar 

  133. Benardo L. S. (1994) Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro. J Physiol 476: 203–215.

    PubMed  CAS  Google Scholar 

  134. Galarreta M. and Hestrin S. (1997) Properties of GABAA receptors underlying inhibitory synaptic currents in neocortical pyramidal neurons. J Neurosci 17: 7220–7227.

    PubMed  CAS  Google Scholar 

  135. Varela J. A., Song S., Turrigiano G. G. and Nelson S. B. (1999) Differential depression at excitatory and inhibitory synapses in visual cortex. J Neurosci 19: 4293–4304.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Brain Mind Institute, EPFL, Lausanne, Switzerland

    Anirudh Gupta, Maria Toledo-Rodriguez, Gilad Silberberg & Henry Markram

Authors
  1. Anirudh Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Toledo-Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gilad Silberberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Henry Markram
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. RIKEN Brain Science Institute, Wako-shi, Japan

    Takao K. Hensch  & Michela Fagiolini  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2003 Springer Science+Business Media New York

About this chapter

Cite this chapter

Gupta, A., Toledo-Rodriguez, M., Silberberg, G., Markram, H. (2003). Interneuron Heterogeneity in Neocortex. In: Hensch, T.K., Fagiolini, M. (eds) Excitatory-Inhibitory Balance. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0039-1_10

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-0039-1_10

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-4895-5

  • Online ISBN: 978-1-4615-0039-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation